Genomic Invasion and the Role of Behaviour in Rapid Evolution

Lay Summary我想要在行动中捕捉到进化，我的提议旨在测试当新的突变“入侵”时基因组会发生什么。这种入侵可能是通过编码或调节基因活性的一段DNA的自发突变，或者通过杂交导致来自另一个种群或物种的基因迁移而发生的。我特别感兴趣的是，有机体根据当时的条件调整其行为的能力如何弥补这种基因组入侵的负面影响，并促进更快速的进化变化。具有选择性优势的新突变的出现和传播是进化过程的核心，但这个过程在自然系统中观察非常具有挑战性，原因有两个：第一，检测到这样的基因组入侵的可能性很小，因为它们发生得如此罕见。第二，进化变化被认为发生的速度非常慢，比研究人员的一生要长得多。我的提议利用了一个教科书上的快速进化例子，这种例子现在正发生在海洋领域的板球--海洋板球(Teleogrolus Ocean Anicus)中。雄性蟋蟀通常会歌唱来吸引雌性蟋蟀交配，但在夏威夷群岛，它们也会吸引一种致命的寄生苍蝇。最近，一种通过消除雄性翅膀上的发声结构使雄性翅膀女性化的突变出现并传播开来。它被称为平翅，存在于两个种群中，似乎具有不同的遗传起源。我的研究将找出这些不同群体的基因组到底发生了什么变化，导致了这种突变的男性类型，并将测试基因组的其他部分是如何反应的。特别是，我将利用来自野外的基因组DNA收集的时间序列来可视化和测试位于物理上与突变密切接近的基因是如何与突变一起被“扫荡”的，或者是如何与基因组的其余部分同质化的。换句话说，当平翅突变侵入大洋锥虫基因组时，可能发生了两件事。第一个是附近的基因被拖着走，现在在种群中被过度代表，第二个是基因组其他部分的基因产生的表型效应对突变特别有效，因此比起正常雄性，突变的雄性更有可能被发现。我从以前的工作中知道，蟋蟀对它们的社会环境特别敏感，特别是对雄性产生的有声歌曲的存在与否。雌性和雄性都会改变交配行为，以适应当时的社会条件，我将测试这一假设，即扁平翅突变能够更快地传播，以响应来自寄生蜂的选择，因为社会灵活性使蟋蟀能够应对变化的社会环境，即出现的沉默环境变得更多。我在实验室里设计了一个蟋蟀跟踪装置，它模拟了野生环境，我可以用它来测试蟋蟀的行为和交配成功。它包括视频和音频记录蟋蟀，使我能够操纵相互作用的个人在试验期间的组成。通过这种方式，我可以改变蟋蟀的社会经验，它们来自什么种群，以及不同形态的相对丰富程度，以测试社会灵活性如何有助于突变雄性的繁殖成功。这些试验的结果将阐明行为如何与进化过程相互作用，以及进化变化的速度如何受到社会环境和个体有机体对该环境的反应的影响。

LAY SUMMARYI want to catch evolution in the act, and my proposal aims to test what happens to genomes when novel mutations "invade". Such an invasion could occur through spontaneous mutation in a section of DNA that codes for or regulates the activity of a gene, or by migration of genes from another population or species due to hybridization. I am particularly interested in how the ability of an organism to adjust its behaviour depending on the prevailing conditions might compensate for negative effects of such a genomic invasion and facilitate more rapid evolutionary change.The emergence and spread of new mutations with a selective advantage is at the heart of the evolutionary process, but this process is extraordinarily challenging to observe in a natural system for two reasons: the first is that the likelihood of detecting such a genomic invasion is miniscule because they happen so rarely. The second is that evolutionary change has been thought to occur at a very slow pace, much longer than a researcher's lifetime. My proposal capitalises on a textbook example of rapid evolution that is occurring right now in the Oceanic field cricket, Teleogryllus oceanicus. Male crickets usually sing to attract females for mating, but in the Hawaiian archipelago, they also attract a deadly parasitoid fly (Ormia ochracea). Recently, a mutation that feminises male wings by erasing sound-producing structures on male wings arose and spread. It is called flatwing, and it exists in two populations and appears to have different genetic origins. My research will work out what, exactly, has changed in the genome of these different populations to cause this mutant male type, and it will test how the rest of the genome has responded. In particular, I will make use of a time-series of genomic DNA collections from the wild to visualise and test how the genes that lie in close physical proximity to the mutation get "swept" along with it, or become homogenized with the rest of the genome. In other words, when the flatwing mutation invaded the T. oceanicus genome, two things may have happened. The first is that genes nearby got dragged along and are now over-represented in the population, and the second is that genes in other parts of the genome produced phenotypic effects that worked particularly well with the mutation, and therefore are more likely to be found in the mutant variety of males than in normal males.I know from previous work that crickets are sensitive to their social environment, in particular, to the presence or absence of acoustic songs that males produce. Both females and males change their mating behaviour to suit the prevailing social conditions, and I will test the hypothesis that the flatwing mutation was able to spread in response to selection from parasitoids more rapidly because social flexibility enabled crickets to cope with the changed social environment, namely, the silent environment that emerged as flatwings became more numerous. I have devised a cricket tracking setup in the lab, which replicates the wild environment and which I can use to test cricket behaviour and mating success. It involves video and audio recording crickets, and enables me to manipulate the composition of interacting individuals during trials. In this manner, I can vary crickets' social experience, what population they are from, and the relative abundance of the different morphs, to test how social flexibility contributes to the reproductive success of mutant males. Results from these trials stand to illuminate how behaviour interacts with the evolutionary process, and how the rate of evolutionary change can be affected by the social environment and individual organisms' responses to that environment.